Interaction between microbiota and immunity in health and disease

Abstract

The interplay between the commensal microbiota and the mammalian immune system development and function includes multifold interactions in homeostasis and disease. The microbiome plays critical roles in the training and development of major components of the host’s innate and adaptive immune system, while the immune system orchestrates the maintenance of key features of host-microbe symbiosis. In a genetically susceptible host, imbalances in microbiota-immunity interactions under defined environmental contexts are believed to contribute to the pathogenesis of a multitude of immune-mediated disorders. Here, we review features of microbiome-immunity crosstalk and their roles in health and disease, while providing examples of molecular mechanisms orchestrating these interactions in the intestine and extra-intestinal organs. We highlight aspects of the current knowledge, challenges and limitations in achieving causal understanding of host immune-microbiome interactions, as well as their impact on immune-mediated diseases, and discuss how these insights may translate towards future development of microbiome-targeted therapeutic interventions.

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     Martinez-Lopez M, et al. Microbiota sensing by Mincle-Syk axis in dendritic cells regulates interleukin-17 and -22 production and promotes intestinal barrier integrity. Immunity. 2019;50:446-461.

     Not in our library10.1016/j.immuni.2018.12.020

123. 123.

     Jie Z, et al. NIK signaling axis regulates dendritic cell function in intestinal immunity and homeostasis. Nat. Immunol. 2018;19:1224-1235.

     Not in our library10.1038/s41590-018-0206-z

124. 124.

     Wingender G, et al. Neutrophilic granulocytes modulate invariant NKT cell function in mice and humans. J. Immunol. 2012;188:3000-3008.

     Not in our library10.4049/jimmunol.1101273

125. 125.

     An D, et al. Sphingolipids from a symbiotic microbe regulate homeostasis of host intestinal natural killer T cells. Cell. 2014;156:123-133.

     Not in our library10.1016/j.cell.2013.11.042

126. 126.

     Rothschild D, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature. 2018;555:210-215.

     Not in our library10.1038/nature25973

127. 127.

     Vojdani A. A potential link between environmental triggers and autoimmunity. Autoimmune Dis. 2014;2014:437231.

     Not in our library10.1155/2014/437231

128. 128.

     Yamamoto-Hanada K, Yang L, Narita M, Saito H, Ohya Y. Influence of antibiotic use in early childhood on asthma and allergic diseases at age 5. Ann. Allergy Asthma Immunol. 2017;119:54-58.

     Not in our library10.1016/j.anai.2017.05.013

129. 129.

     Becattini S, Taur Y, Pamer EG. Antibiotic-induced changes in the intestinal microbiota and disease. Trends Mol. Med. 2016;22:458-478.

     Not in our library10.1016/j.molmed.2016.04.003

130. 130.

     Sato H, et al. Antibiotics suppress activation of intestinal mucosal mast cells and reduce dietary lipid absorption in Sprague-Dawley rats. Gastroenterology. 2016;151:923-932.

     Not in our library10.1053/j.gastro.2016.07.009

131. 131.

     Scott NA, et al. Antibiotics induce sustained dysregulation of intestinal T cell immunity by perturbing macrophage homeostasis. Sci. Transl. Med. 2018;10:eaao4755.

     Not in our library10.1126/scitranslmed.aao4755

132. 132.

     Kim YG, et al. Gut dysbiosis promotes M2 macrophage polarization and allergic airway inflammation via fungi-induced PGE(2). Cell Host Microbe. 2014;15:95-102.

     Not in our library10.1016/j.chom.2013.12.010

133. 133.

     Kim M, et al. Critical Role for the microbiota in CX3CR1(+) intestinal mononuclear phagocyte regulation of intestinal T cell responses. Immunity. 2018;49:151-163.

     Not in our library10.1016/j.immuni.2018.05.009

134. 134.

     Ohnmacht C, et al. MUCOSAL IMMUNOLOGY. The microbiota regulates type 2 immunity through RORgammat(+) T cells. Science. 2015;349:989-993.

     Not in our library10.1126/science.aac4263

135. 135.

     Hagan T, et al. Antibiotics-driven gut microbiome perturbation alters immunity to vaccines in humans. Cell. 2019;178:1313-1328.

     Not in our library10.1016/j.cell.2019.08.010

136. 136.

     Christ A, Lauterbach M, Latz E. Western diet and the immune system: An inflammatory connection. Immunity. 2019;51:794-811.

     Not in our library10.1016/j.immuni.2019.09.020

137. 137.

     Devkota S, et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10−/− mice. Nature. 2012;487:104-108.

     Not in our library10.1038/nature11225

138. 138.

     Cheng L, et al. High fat diet exacerbates dextran sulfate sodium induced colitis through disturbing mucosal dendritic cell homeostasis. Int. Immunopharmacol. 2016;40:1-10.

     Not in our library10.1016/j.intimp.2016.08.018

139. 139.

     Haghikia A, et al. Dietary fatty acids directly impact central nervous system autoimmunity via the small intestine. Immunity. 2015;43:817-829.

     Not in our library10.1016/j.immuni.2015.09.007

140. 140.

     He B, et al. Resetting microbiota by Lactobacillus reuteri inhibits T reg deficiency-induced autoimmunity via adenosine A2A receptors. J. Exp. Med. 2017;214:107-123.

     Not in our library10.1084/jem.20160961

141. 141.

     Rodriguez-Palacios A, et al. The artificial sweetener splenda promotes gut Proteobacteria, dysbiosis, and myeloperoxidase reactivity in Crohn’s disease-like ileitis. Inflamm. Bowel Dis. 2018;24:1005-1020.

     Not in our library10.1093/ibd/izy060

142. 142.

     Viennois E, Merlin D, Gewirtz AT, Chassaing B. Dietary emulsifier-induced low-grade inflammation promotes colon carcinogenesis. Cancer Res. 2017;77:27-40.

     Not in our library10.1158/0008-5472.can-16-1359

143. 143.

     Martinez I, et al. Gut microbiome composition is linked to whole grain-induced immunological improvements. ISME J. 2013;7:269-280.

     Not in our library10.1038/ismej.2012.104

144. 144.

     Cignarella F, et al. Intermittent fasting confers protection in CNS autoimmunity by altering the gut microbiota. Cell Metab. 2018;27:1222-1235.

     Not in our library10.1016/j.cmet.2018.05.006

145. 145.

     Rangan P, et al. Fasting-mimicking diet modulates microbiota and promotes intestinal regeneration to reduce inflammatory bowel disease pathology. Cell Rep. 2019;26:2704-2719.

     Not in our library10.1016/j.celrep.2019.02.019

146. 146.

     Bishehsari F, et al. Abnormal eating patterns cause circadian disruption and promote alcohol-associated colon carcinogenesis. Cell Mol. Gastroenterol. Hepatol. 2020;9:219-237.

     Not in our library10.1016/j.jcmgh.2019.10.011

147. 147.

     Rosshart SP, et al. Laboratory mice born to wild mice have natural microbiota and model human immune responses. Science. 2019;365:eaaw4361.

     Not in our library10.1126/science.aaw4361

148. 148.

     Kaplan GG. The global burden of IBD: from 2015 to 2025. Nat. Rev. Gastroenterol. Hepatol. 2015;12:720-727.

     Not in our library10.1038/nrgastro.2015.150

149. 149.

     Kostic AD, Xavier RJ, Gevers D. The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology. 2014;146:1489-1499.

     Not in our library10.1053/j.gastro.2014.02.009

150. 150.

     Gevers D, et al. The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe. 2014;15:382-392.

     Not in our library10.1016/j.chom.2014.02.005

151. 151.

     Franzosa EA, et al. Gut microbiome structure and metabolic activity in inflammatory bowel disease. Nat. Microbiol. 2019;4:293-305.

     Not in our library10.1038/s41564-018-0306-4

152. 152.
     Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases · 2019

     No notice
153. 153.

     de Souza HS, Fiocchi C. Immunopathogenesis of IBD: current state of the art. Nat. Rev. Gastroenterol. Hepatol. 2016;13:13-27.

     Not in our library10.1038/nrgastro.2015.186

154. 154.
     Mend Your FencesSummary · 2017

     Not checked
155. 155.

     Van der Sluis M, et al. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology. 2006;131:117-129.

     Not in our library10.1053/j.gastro.2006.04.020

156. 156.

     Liso M, et al. A specific mutation in Muc2 determines early dysbiosis in colitis-prone Winnie mice. Inflamm. Bowel Dis. 2020;26:546-556.

     Not in our library10.1093/ibd/izz279

157. 157.

     Ogura Y, et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn’s disease. Nature. 2001;411:603-606.

     Not in our library10.1038/35079114

158. 158.

     Hugot JP, et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn’s disease. Nature. 2001;411:599-603.

     Not in our library10.1038/35079107

159. 159.

     Petnicki-Ocwieja T, et al. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc. Natl. Acad. Sci. USA. 2009;106:15813-15818.

     Not in our library10.1073/pnas.0907722106

160. 160.

     Cadwell K, et al. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature. 2008;456:259-263.

     Not in our library10.1038/nature07416

161. 161.
     ATG16L1 orchestrates interleukin-22 signaling in the intestinal epithelium via cGAS–STING · 2018

     No notice
162. 162.

     Seregin SS, et al. NLRP6 protects Il10(−/−) mice from colitis by limiting colonization of Akkermansia muciniphila. Cell Rep. 2017;19:733-745.

     Not in our library10.1016/j.celrep.2017.03.080

163. 163.

     Schaubeck M, et al. Dysbiotic gut microbiota causes transmissible Crohn’s disease-like ileitis independent of failure in antimicrobial defence. Gut. 2016;65:225-237.

     Not in our library10.1136/gutjnl-2015-309333

164. 164.

     Britton GJ, et al. Microbiotas from humans with inflammatory bowel disease alter the balance of gut Th17 and RORgammat(+) regulatory T cells and exacerbate colitis in mice. Immunity. 2019;50:212-224.

     Not in our library10.1016/j.immuni.2018.12.015

165. 165.

     Caruso R, et al. A specific gene-microbe interaction drives the development of Crohn’s disease-like colitis in mice. Sci. Immunol. 2019;4:eaaw4341.

     Not in our library10.1126/sciimmunol.aaw4341

166. 166.

     Atarashi K, et al. Ectopic colonization of oral bacteria in the intestine drives TH1 cell induction and inflammation. Science. 2017;358:359-365.

     Not in our library10.1126/science.aan4526

167. 167.

     Torres J, et al. Infants born to mothers with IBD present with altered gut microbiome that transfers abnormalities of the adaptive immune system to germ-free mice. Gut. 2020;69:42-51.

     Not in our library10.1136/gutjnl-2018-317855

168. 168.
     Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis · 2013

     No notice
169. 169.

     Maeda Y, et al. Dysbiosis contributes to arthritis development via activation of autoreactive T cells in the intestine. Arthritis Rheumatol. 2016;68:2646-2661.

     Not in our library10.1002/art.39783

170. 170.

     Alpizar-Rodriguez D, et al. Prevotella copri in individuals at risk for rheumatoid arthritis. Ann. Rheum. Dis. 2019;78:590-593.

     Not in our library10.1136/annrheumdis-2018-214514

171. 171.
     An expansion of rare lineage intestinal microbes characterizes rheumatoid arthritis · 2016

     No notice
172. 172.

     Zhang X, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat. Med. 2015;21:895-905.

     Not in our library10.1038/nm.3914

173. 173.

     Wang Q, Xu R. Data-driven multiple-level analysis of gut-microbiome-immune-joint interactions in rheumatoid arthritis. BMC Genom. 2019;20:124.

     Not in our library10.1186/s12864-019-5510-y

174. 174.

     Abdollahi-Roodsaz S, et al. Stimulation of TLR2 and TLR4 differentially skews the balance of T cells in a mouse model of arthritis. J. Clin. Invest. 2008;118:205-216.

     Not in our library10.1172/jci32639

175. 175.

     Rogier R, et al. Aberrant intestinal microbiota due to IL-1 receptor antagonist deficiency promotes IL-17- and TLR4-dependent arthritis. Microbiome. 2017;5:63.

     Not in our library10.1186/s40168-017-0278-2

176. 176.

     Wu HJ, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity. 2010;32:815-827.

     Not in our library10.1016/j.immuni.2010.06.001

177. 177.

     de Aquino SG, et al. Periodontal pathogens directly promote autoimmune experimental arthritis by inducing a TLR2- and IL-1-driven Th17 response. J. Immunol. 2014;192:4103-4111.

     Not in our library10.4049/jimmunol.1301970

178. 178.

     Hotamisligil GS. Inflammation, metaflammation and immunometabolic disorders. Nature. 2017;542:177-185.

     Not in our library10.1038/nature21363

179. 179.

     Tilg H, Zmora N, Adolph TE, Elinav E. The intestinal microbiota fuelling metabolic inflammation. Nat. Rev. Immunol. 2020;20:40-54.

     Not in our library10.1038/s41577-019-0198-4

180. 180.
     The role of the microbiome in NAFLD and NASH · 2018

     No notice
181. 181.

     Henao-Mejia J, et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature. 2012;482:179-185.

     Not in our library10.1038/nature10809

182. 182.

     Bodogai M, et al. Commensal bacteria contribute to insulin resistance in aging by activating innate B1a cells. Sci. Transl. Med. 2018;10:eaat4271.

     Not in our library10.1126/scitranslmed.aat4271

183. 183.

     Virtue AT, et al. The gut microbiota regulates white adipose tissue inflammation and obesity via a family of microRNAs. Sci. Transl. Med. 2019;11:eaav1892.

     Not in our library10.1126/scitranslmed.aav1892

184. 184.

     Truax AD, et al. The inhibitory innate immune sensor NLRP12 maintains a threshold against obesity by regulating gut microbiota homeostasis. Cell Host Microbe. 2018;24:364-378.

     Not in our library10.1016/j.chom.2018.08.009

185. 185.

     Koeth RA, et al. l-Carnitine in omnivorous diets induces an atherogenic gut microbial pathway in humans. J. Clin. Invest. 2019;129:373-387.

     Not in our library10.1172/jci94601

186. 186.

     Wang Z, et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature. 2011;472:57-63.

     Not in our library10.1038/nature09922

187. 187.

     Gur C, et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity. 2015;42:344-355.

     Not in our library10.1016/j.immuni.2015.01.010

188. 188.

     Mima K, et al. Fusobacterium nucleatum and T cells in colorectal carcinoma. JAMA Oncol. 2015;1:653-661.

     Not in our library10.1001/jamaoncol.2015.1377

189. 189.

     Ma C, et al. Gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells. Science. 2018;360:eaan5931.

     Not in our library10.1126/science.aan5931

190. 190.

     Matson V, et al. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science. 2018;359:104-108.

     Not in our library10.1126/science.aao3290

191. 191.

     Gopalakrishnan V, et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science. 2018;359:97-103.

     Not in our library10.1126/science.aan4236

192. 192.

     Sivan A, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science. 2015;350:1084-1089.

     Not in our library10.1126/science.aac4255

193. 193.

     Routy B, et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science. 2018;359:91-97.

     Not in our library10.1126/science.aan3706

194. 194.

     Vetizou M, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015;350:1079-1084.

     Not in our library10.1126/science.aad1329

195. 195.

     Viaud S, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science. 2013;342:971-976.

     Not in our library10.1126/science.1240537

196. 196.

     Zitvogel L, Ayyoub M, Routy B, Kroemer G. Microbiome and anticancer immunosurveillance. Cell. 2016;165:276-287.

     Not in our library10.1016/j.cell.2016.03.001

197. 197.

     Pushalkar S, et al. The pancreatic cancer microbiome promotes oncogenesis by induction of innate and adaptive immune suppression. Cancer Discov. 2018;8:403-416.

     Not in our library10.1158/2159-8290.cd-17-1134

198. 198.

     Geller LT, et al. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine. Science. 2017;357:1156-1160.

     Not in our library10.1126/science.aah5043

199. 199.

     Riquelme E, et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell. 2019;178:795-806.

     Not in our library10.1016/j.cell.2019.07.008

200. 200.

     Grice EA, et al. Topographical and temporal diversity of the human skin microbiome. Science. 2009;324:1190-1192.

     Not in our library10.1126/science.1171700

201. 201.

     Oh J, Byrd AL, Park M, Kong HH, Segre JA. Temporal stability of the human skin microbiome. Cell. 2016;165:854-866.

     Not in our library10.1016/j.cell.2016.04.008

202. 202.

     Oh J, et al. Biogeography and individuality shape function in the human skin metagenome. Nature. 2014;514:59-64.

     Not in our library10.1038/nature13786

203. 203.

     Chehoud C, et al. Complement modulates the cutaneous microbiome and inflammatory milieu. Proc. Natl. Acad. Sci. USA. 2013;110:15061-15066.

     Not in our library10.1073/pnas.1307855110

204. 204.
     Endogenous Antimicrobial Peptide Expression in Response to Bacterial Epidermal Colonization · 2017

     Not checked
205. 205.

     Naik S, et al. Commensal-dendritic-cell interaction specifies a unique protective skin immune signature. Nature. 2015;520:104-108.

     Not in our library10.1038/nature14052

206. 206.

     Linehan JL, et al. Non-classical immunity controls microbiota impact on skin immunity and tissue repair. Cell. 2018;172:784-796.

     Not in our library10.1016/j.cell.2017.12.033

207. 207.

     Lai Y, et al. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat. Med. 2009;15:1377-1382.

     Not in our library10.1038/nm.2062

208. 208.

     Scharschmidt TC, et al. A wave of regulatory T cells into neonatal skin mediates tolerance to commensal microbes. Immunity. 2015;43:1011-1021.

     Not in our library10.1016/j.immuni.2015.10.016

209. 209.

     Scharschmidt TC, et al. Commensal microbes and hair follicle morphogenesis coordinately drive Treg migration into neonatal skin. Cell Host Microbe. 2017;21:467-477.

     Not in our library10.1016/j.chom.2017.03.001

210. 210.

     Sanford JA, et al. Inhibition of HDAC8 and HDAC9 by microbial short-chain fatty acids breaks immune tolerance of the epidermis to TLR ligands. Sci. Immunol. 2016;1:eaah4609.

     Not in our library10.1126/sciimmunol.aah4609

211. 211.

     Nakatsuji T, et al. Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Sci. Transl. Med. 2017;9:eaah4680.

     Not in our library10.1126/scitranslmed.aah4680

212. 212.

     Kong HH, et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res. 2012;22:850-859.

     Not in our library10.1101/gr.131029.111

213. 213.

     Stehlikova Z, et al. Dysbiosis of skin microbiota in Psoriatic patients: co-occurrence of fungal and bacterial communities. Front. Microbiol. 2019;10:438.

     Not in our library10.3389/fmicb.2019.00438

214. 214.

     Belkaid Y, Segre JA. Dialogue between skin microbiota and immunity. Science. 2014;346:954-959.

     Not in our library10.1126/science.1260144

215. 215.

     Nakamura Y, et al. Staphylococcus delta-toxin induces allergic skin disease by activating mast cells. Nature. 2013;503:397-401.

     Not in our library10.1038/nature12655

216. 216.

     Uluckan O, et al. Cutaneous immune cell-microbiota interactions are controlled by epidermal JunB/AP-1. Cell Rep. 2019;29:844-859.

     Not in our library10.1016/j.celrep.2019.09.042

217. 217.

     Ichinohe T, et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl. Acad. Sci. USA. 2011;108:5354-5359.

     Not in our library10.1073/pnas.1019378108

218. 218.

     Fagundes CT, et al. Transient TLR activation restores inflammatory response and ability to control pulmonary bacterial infection in germfree mice. J. Immunol. 2012;188:1411-1420.

     Not in our library10.4049/jimmunol.1101682

219. 219.

     Trompette A, et al. Dietary fiber confers protection against flu by shaping Ly6c(−) patrolling monocyte hematopoiesis and CD8(+) T cell metabolism. Immunity. 2018;48:992-1005.

     Not in our library10.1016/j.immuni.2018.04.022

220. 220.

     Steed AL, et al. The microbial metabolite desaminotyrosine protects from influenza through type I interferon. Science. 2017;357:498-502.

     Not in our library10.1126/science.aam5336

221. 221.

     Marsland BJ, Gollwitzer ES. Host-microorganism interactions in lung diseases. Nat. Rev. Immunol. 2014;14:827-835.

     Not in our library10.1038/nri3769

222. 222.

     Gollwitzer ES, et al. Lung microbiota promotes tolerance to allergens in neonates via PD-L1. Nat. Med. 2014;20:642-647.

     Not in our library10.1038/nm.3568

223. 223.

     Pattaroni C, et al. Early-life formation of the microbial and immunological environment of the human airways. Cell Host Microbe. 2018;24:857-865.

     Not in our library10.1016/j.chom.2018.10.019

224. 224.

     Dickson RP, Martinez FJ, Huffnagle GB. The role of the microbiome in exacerbations of chronic lung diseases. Lancet. 2014;384:691-702.

     Not in our library10.1016/s0140-6736(14)61136-3

225. 225.

     Yadava K, et al. Microbiota promotes chronic pulmonary inflammation by enhancing IL-17A and autoantibodies. Am. J. Respir. Crit. Care Med. 2016;193:975-987.

     Not in our library10.1164/rccm.201504-0779oc

226. 226.

     Segal LN, et al. Enrichment of the lung microbiome with oral taxa is associated with lung inflammation of a Th17 phenotype. Nat. Microbiol. 2016;1:16031.

     Not in our library10.1038/nmicrobiol.2016.31

227. 227.

     Larsen JM, et al. Chronic obstructive pulmonary disease and asthma-associated Proteobacteria, but not commensal Prevotella spp., promote Toll-like receptor 2-independent lung inflammation and pathology. Immunology. 2015;144:333-342.

     Not in our library10.1111/imm.12376

228. 228.

     Jin C, et al. Commensal microbiota promote lung cancer development via gammadelta T cells. Cell. 2019;176:998-1013.

     Not in our library10.1016/j.cell.2018.12.040

229. 229.

     Corbitt N, et al. Gut bacteria drive Kupffer cell expansion via MAMP-mediated ICAM-1 induction on sinusoidal endothelium and influence preservation-reperfusion injury after orthotopic liver transplantation. Am. J. Pathol. 2013;182:180-191.

     Not in our library10.1016/j.ajpath.2012.09.010

230. 230.

     Chen J, et al. Natural killer T cells play a necessary role in modulating of immune-mediated liver injury by gut microbiota. Sci. Rep. 2014;4:7259.

     Not in our library10.1038/srep07259

231. 231.

     Liang S, Webb T, Li Z. Probiotic antigens stimulate hepatic natural killer T cells. Immunology. 2014;141:203-210.

     Not in our library10.1111/imm.12180

232. 232.

     Paik YH, et al. Toll-like receptor 4 mediates inflammatory signaling by bacterial lipopolysaccharide in human hepatic stellate cells. Hepatology. 2003;37:1043-1055.

     Not in our library10.1053/jhep.2003.50182

233. 233.

     Nakamoto N, et al. Gut pathobionts underlie intestinal barrier dysfunction and liver T helper 17 cell immune response in primary sclerosing cholangitis. Nat. Microbiol. 2019;4:492-503.

     Not in our library10.1038/s41564-018-0333-1

234. 234.

     Liwinski T, et al. Alterations of the bile microbiome in primary sclerosing cholangitis. Gut. 2020;69:665-672.

     Not in our library10.1136/gutjnl-2019-318416

235. 235.

     Yoshimoto S, et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature. 2013;499:97-101.

     Not in our library10.1038/nature12347

236. 236.

     Loo TM, et al. Gut microbiota promotes obesity-associated liver cancer through PGE2-mediated suppression of antitumor immunity. Cancer Discov. 2017;7:522-538.

     Not in our library10.1158/2159-8290.cd-16-0932

237. 237.

     Dapito DH, et al. Promotion of hepatocellular carcinoma by the intestinal microbiota and TLR4. Cancer Cell. 2012;21:504-516.

     Not in our library10.1016/j.ccr.2012.02.007

238. 238.

     Sharon G, Sampson TR, Geschwind DH, Mazmanian SK. The central nervous system and the gut microbiome. Cell. 2016;167:915-932.

     Not in our library10.1016/j.cell.2016.10.027

239. 239.

     Butovsky O, Weiner HL. Microglial signatures and their role in health and disease. Nat. Rev. Neurosci. 2018;19:622-635.

     Not in our library10.1038/s41583-018-0057-5

240. 240.

     Erny D, et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci. 2015;18:965-977.

     Not in our library10.1038/nn.4030

241. 241.

     Matcovitch-Natan O, et al. Microglia development follows a stepwise program to regulate brain homeostasis. Science. 2016;353:aad8670.

     Not in our library10.1126/science.aad8670

242. 242.
     Microbiome Influences Prenatal and Adult Microglia in a Sex-Specific Manner · 2018

     No notice
243. 243.

     Abdel-Haq R, Schlachetzki JCM, Glass CK, Mazmanian SK. Microbiome-microglia connections via the gut-brain axis. J. Exp. Med. 2019;216:41-59.

     Not in our library10.1084/jem.20180794

244. 244.

     Benakis C, et al. Commensal microbiota affects ischemic stroke outcome by regulating intestinal gammadelta T cells. Nat. Med. 2016;22:516-523.

     Not in our library10.1038/nm.4068

245. 245.

     Ochoa-Reparaz J, et al. Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. J. Immunol. 2009;183:6041-6050.

     Not in our library10.4049/jimmunol.0900747

246. 246.

     Kim S, et al. Maternal gut bacteria promote neurodevelopmental abnormalities in mouse offspring. Nature. 2017;549:528-532.

     Not in our library10.1038/nature23910

247. 247.

     Reed MD, et al. IL-17a promotes sociability in mouse models of neurodevelopmental disorders. Nature. 2020;577:249-253.

     Not in our library10.1038/s41586-019-1843-6

248. 248.

     Yang D, et al. Dysregulated lung commensal bacteria drive interleukin-17B production to promote pulmonary fibrosis through their outer membrane vesicles. Immunity. 2019;50:692-706.

     Not in our library10.1016/j.immuni.2019.02.001

249. 249.

     O’Callaghan JL, et al. Re-assessing microbiomes in the low-biomass reproductive niche. BJOG. 2020;127:147-158.

     Not in our library10.1111/1471-0528.15974

250. 250.
     KatharoSeq Enables High-Throughput Microbiome Analysis from Low-Biomass Samples · 2018

     No notice
251. 251.
     Reagent and laboratory contamination can critically impact sequence-based microbiome analyses · 2014

     No notice
252. 252.

     de Goffau MC, et al. Human placenta has no microbiome but can contain potential pathogens. Nature. 2019;572:329-334.

     Not in our library10.1038/s41586-019-1451-5

253. 253.

     Kuperman AA, et al. Deep microbial analysis of multiple placentas shows no evidence for a placental microbiome. BJOG. 2020;127:159-169.

     Not in our library10.1111/1471-0528.15896

254. 254.
     Controlling for Contaminants in Low-Biomass 16S rRNA Gene Sequencing Experiments · 2019

     No notice
255. 255.

     Burnham P, et al. Separating the signal from the noise in metagenomic cell-free DNA sequencing. Microbiome. 2020;8:18.

     Not in our library10.1186/s40168-020-0793-4

256. 256.

     Eisenhofer R, et al. Contamination in low microbial biomass microbiome studies: Issues and recommendations. Trends Microbiol. 2019;27:105-117.

     Not in our library10.1016/j.tim.2018.11.003

257. 257.

     Limon JJ, et al. Malassezia is associated with Crohn’s disease and exacerbates colitis in mouse models. Cell Host Microbe. 2019;25:377-388.

     Not in our library10.1016/j.chom.2019.01.007

258. 258.

     Sokol H, et al. Fungal microbiota dysbiosis in IBD. Gut. 2017;66:1039-1048.

     Not in our library10.1136/gutjnl-2015-310746

259. 259.

     Norman JM, et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell. 2015;160:447-460.

     Not in our library10.1016/j.cell.2015.01.002

260. 260.

     Zuo T, et al. Gut mucosal virome alterations in ulcerative colitis. Gut. 2019;68:1169-1179.

     Not in our library10.1136/gutjnl-2018-318131

261. 261.

     Liu TC, Stappenbeck TS. Genetics and pathogenesis of inflammatory bowel disease. Annu. Rev. Pathol. 2016;11:127-148.

     Not in our library10.1146/annurev-pathol-012615-044152

262. 262.

     Rosshart SP, et al. Wild mouse gut microbiota promotes host fitness and improves disease resistance. Cell. 2017;171:1015-1028.

     Not in our library10.1016/j.cell.2017.09.016

263. 263.

     Tanoue T, et al. A defined commensal consortium elicits CD8 T cells and anti-cancer immunity. Nature. 2019;565:600-605.

     Not in our library10.1038/s41586-019-0878-z

264. 264.

     Zhu W, et al. Precision editing of the gut microbiota ameliorates colitis. Nature. 2018;553:208-211.

     Not in our library10.1038/nature25172

265. 265.
     Interactions between Bacteriophage, Bacteria, and the Mammalian Immune System · 2018

     No notice
266. 266.

     Zeevi D, et al. Personalized nutrition by prediction of glycemic responses. Cell. 2015;163:1079-1094.

     Not in our library10.1016/j.cell.2015.11.001

267. 267.

     Levy M, Thaiss CA, Elinav E. Metabolites: messengers between the microbiota and the immune system. Genes Dev. 2016;30:1589-1597.

     Not in our library10.1101/gad.284091.116

268. 268.

     Chen H, et al. A forward chemical genetic screen reveals gut microbiota metabolites that modulate host physiology. Cell. 2019;177:1217-1231.

     Not in our library10.1016/j.cell.2019.03.036

Cited by papers we hold 57

• Gut modulation to regulate NF-κB in colorectal and gastric cancer therapy and inflammation · 2025
  Not checked
• Multiomics analyses of gut microbiota and metabolites in people living with HIV before and during SARS-COV-2 infection · 2025
  Not checked
• Type 2 immunity in allergic diseases · 2025
  No notice
• The microbiome in graft-versus-host disease: a tale of two ecosystems · 2025
  Not checked
• Beyond the gut: decoding the gut–immune–brain axis in health and disease · 2025
  No notice
• Gut Microbiota Dysbiosis: Pathogenesis, Diseases, Prevention, and Therapy · 2025
  No notice
• Host genetic regulation of human gut microbial structural variation · 2024
  No notice
• Breaking the barriers: the role of gut homeostasis in Metabolic-Associated Steatotic Liver Disease (MASLD) · 2024
  No notice
• Navigating Challenges and Opportunities in Multi-Omics Integration for Personalized Healthcare · 2024
  No notice
• Intratumoural microbiota: a new frontier in cancer development and therapy · 2024
  No notice
• Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases · 2024
  No notice
• The gut microbiota–brain axis in neurological disorder · 2023
  No notice
• Excessive consumption of mucin by over-colonized Akkermansia muciniphila promotes intestinal barrier damage during malignant intestinal environment · 2023
  No notice
• Deficient butyrate-producing capacity in the gut microbiome is associated with bacterial network disturbances and fatigue symptoms in ME/CFS · 2023
  No notice
• Signalling cognition: the gut microbiota and hypothalamic-pituitary-adrenal axis · 2023
  No notice
• Understanding the Gut–Brain Axis and Its Therapeutic Implications for Neurodegenerative Disorders · 2023
  No notice
• Roles of Short-Chain Fatty Acids in Inflammatory Bowel Disease · 2023
  No notice
• Crosstalk between Gut Microbiota and Host Immunity: Impact on Inflammation and Immunotherapy · 2023
  No notice
• The Notch signaling pathway: a potential target for cancer immunotherapy · 2023
  No notice
• Probiotics Mechanism of Action on Immune Cells and Beneficial Effects on Human Health · 2023
  No notice

and 37 more

Reads

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